Differential selection on carotenoid biosynthesis genes as a function of gene position in the metabolic pathway: a study on the carrot and dicots

• Published in: PloS one Vol. 7; no. 6; p. e38724
• Main Authors: Clotault, Jérémy, Peltier, Didier, Soufflet-Freslon, Vanessa, Briard, Mathilde, Geoffriau, Emmanuel
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 18-06-2012; Public Library of Science (PLoS)
• Subjects: Acids; Agriculture; Arabidopsis Proteins - genetics; Arabidopsis thaliana; Bayes Theorem; Biological evolution; Biology; Biosynthesis; Breeding; Carotenoids; Carotenoids - metabolism; Carrots; cis-trans-Isomerases - genetics; Comparative analysis; Cultivation; Daucus carota; Daucus carota - genetics; Domestication; Enzymes; Evolution & development; Evolution, Molecular; Fines & penalties; Fluxes; Fruits; Gene sequencing; Genes; Genes, Plant; Genetic polymorphisms; Genetic research; Genetics; Genetics, Population; Geography; Horticulture; Life Sciences; Metabolic pathways; Metabolism; Methods; Models, Biological; Models, Genetic; Mutation; Neural networks; Nucleotides - genetics; Phylogenetics; Phylogeny; Physiological aspects; Plant Physiological Phenomena; Plant Roots - genetics; Polymorphism, Genetic; Population genetics; Principal Component Analysis; Proteins; Studies; Surveys; Taxa; Vegetal Biology; France; FSH
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0038724

Selection of genes involved in metabolic pathways could target them differently depending on the position of genes in the pathway and on their role in controlling metabolic fluxes. This hypothesis was tested in the carotenoid biosynthesis pathway using population genetics and phylogenetics.
Evolutionary rates of seven genes distributed along the carotenoid biosynthesis pathway, IPI, PDS, CRTISO, LCYB, LCYE, CHXE and ZEP, were compared in seven dicot taxa. A survey of deviations from neutrality expectations at these genes was also undertaken in cultivated carrot (Daucus carota subsp. sativus), a species that has been intensely bred for carotenoid pattern diversification in its root during its cultivation history. Parts of sequences of these genes were obtained from 46 individuals representing a wide diversity of cultivated carrots. Downstream genes exhibited higher deviations from neutral expectations than upstream genes. Comparisons of synonymous and nonsynonymous substitution rates between genes among dicots revealed greater constraints on upstream genes than on downstream genes. An excess of intermediate frequency polymorphisms, high nucleotide diversity and/or high differentiation of CRTISO, LCYB1 and LCYE in cultivated carrot suggest that balancing selection may have targeted genes acting centrally in the pathway.
Our results are consistent with relaxed constraints on downstream genes and selection targeting the central enzymes of the carotenoid biosynthesis pathway during carrot breeding history.